Diversity and evolution of bodyguard manipulation. Fanny Maure, Simon Payette Daoust, Jacques Brodeur, Guillaume Mitta, Frédéric Thomas

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Fanny Maure, Simon Payette Daoust, Jacques Brodeur, Guillaume Mitta, Frédéric Thomas. Diversity and evolution of bodyguard manipulation.. Journal of Experimental Biology, Cambridge University Press, 2013, 216 (Pt 1), pp.36-42. ￿10.1242/jeb.073130￿. ￿halsde-00771849￿

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The Journal of Experimental Biology 216, 36-42 © 2013. Published by The Company of Biologists Ltd doi:10.1242/jeb.073130

REVIEW Diversity and evolution of bodyguard manipulation

Fanny Maure1,2,*,†, Simon Payette Daoust1,2,*, Jacques Brodeur2, Guillaume Mitta3 and Frédéric Thomas1 1IRD, MIVEGEC (UMR CNRS/IRD/UM1/UM2), 911 Avenue Agropolis, BP 64501, FR-34394 Montpellier cedex 5, France, 2Institut de recherche en biologie végétale, Département de sciences biologiques, Université de Montréal 4101, rue Sherbrooke est, Montréal, Québec, Canada H1X 2B2 and 3Université de Perpignan Via Domitia, Écologie et Évolution des Interactions (UMR CNRS 5244), 52 Avenue Paul Alduy, 66860 Perpignan cedex, France *These authors contributed equally to this work †Author for correspondence ([email protected])

Summary Among the different strategies used by parasites to usurp the behaviour of their host, one of the most fascinating is bodyguard manipulation. While all classic examples of bodyguard manipulation involve , induced protective behaviours have also evolved in other parasite–host systems, typically as specific dimensions of the total manipulation. For instance, parasites may manipulate the host to reduce host mortality during their development or to avoid predation by non-host predators. This type of host manipulation behaviour is rarely described, probably due to the fact that studies have mainly focused on predation enhancement rather than studying all the dimensions of the manipulation. Here, in addition to the classic cases of bodyguard manipulation, we also review these ʻbodyguard dimensionsʼ and propose extending the current definition of bodyguard manipulation to include the latter. We also discuss different evolutionary scenarios under which such manipulations could have evolved. Keywords: host–parasite relationships, co-evolution, bodyguard manipulation, bodyguard dimension. Received 28 March 2012; Accepted 30 May 2012

Introduction to vertebrate hosts by blood-sucking such as mosquitoes Host manipulation by parasites is one of the most concrete and (Lefèvre et al., 2006). In this situation, transmission opportunities fascinating examples of the extended phenotype (Dawkins, 1982). for the parasite increase with the number of potential hosts visited Parasites across many taxa, from viruses to parasitoids, have by the mosquitoes, and parasites have been shown to shorten the evolved the ability to manipulate their hosts to their own advantage, duration of individual blood meals to increase the number of hosts sometimes inducing spectacular behavioural changes in their hosts attacked (Moore, 1993; Koella et al., 1998). (Moore, 2002; Lefèvre et al., 2009; Poulin, 2010; Hughes et al., The last category of manipulation is known as bodyguard 2012). Although these phenotypic changes occur only in parasitized manipulation. Although fascinating, it remains largely unstudied, hosts, evidence of benefits for the parasites is necessary to allow with only a handful of documented cases and even fewer addressing conclusions to be drawn about their adaptiveness (Poulin, 2010). the underlying mechanisms. This type of manipulation is used by Traditionally, parasitic host manipulations have been divided insect parasitoids that must exit their host following larval into four general categories, three of which have been well development and pupate on external substrates, and is defined by documented (Poulin, 2010). In the first, the parasites can Poulin as ‘a manipulation that alters the behaviour of the host in manipulate their hosts in such a way as to favour transmission to ways that will provide protection to the parasite pupae from their next host, by rendering the former more susceptible to predators or other dangers’ (Poulin, 2010), where the host forgoes predation. One of the best-described examples is that of amphipods potential foraging and/or reproductive opportunities. While all of infected with trematode parasites; infected gammarids display an the documented examples of bodyguard manipulation involve aberrant escape response toward the water surface following a parasitoids and more particularly parasitic , induced mechanical disturbance, and remain at the air–water interface, protective behaviours can evolve in other parasite–host systems. thereby favouring the parasite’s transmission to the definitive host, For instance, within the context of multidimensional manipulations, a waterfowl (Bethel and Holmes, 1977; Helluy, 1983; Helluy, where parasites modify multiple aspects of their host’s phenotype 1984). The second category involves parasites that must either exit (see Appendix), certain dimensions (i.e. aspects) of these the host or release their propagules in a habitat other than the one manipulations have been shown to reduce predation pressure and in which the host lives. For example, crickets Nemobius sylvestris therefore the mortality of the immature parasites. Although infected with the nematomorph Paragordius tricuspidatus were currently labelled as the ‘predation suppression’ phase (see Parker shown to actively jump into pools and streams, where the worms et al., 2009), these behaviours ultimately ensure parasite survival. would egress from the host and find mates (Thomas et al., 2002b). From this point of view, they could be interpreted as ‘bodyguard The third type of manipulation involves vector-borne parasite dimensions’, where manipulated hosts act as bodyguards only transmission. The best-known examples are pathogens transmitted during specific phases of the manipulation.

THE JOURNAL OF EXPERIMENTAL BIOLOGY Bodyguard manipulation 37

The present review examines the diversity and evolution of beetle Coleomegilla maculata (Table1). Female wasps lay a single bodyguard manipulation. First, we will give an overview of the egg in the host and the grows inside the body cavity textbook cases of bodyguard manipulation. Second, we will of the ladybird until it reaches the prepupal stage. Then, the larva highlight the bodyguard dimension that occurs in a great number egresses from its host and begins spinning a cocoon between the of biological systems, and discuss its potential inclusion in a ladybird’s legs (Fig.1C). Remarkably for a parasitoid, D. broader definition of bodyguard manipulation. We will conclude coccinellae does not kill its host at the end of its development; this paper by discussing the evolutionary process leading to instead, it partially paralyses the coccinellid upon egression. Thus bodyguard manipulation. positioned on top of the parasitic cocoon and displaying little twitching when disturbed, the ladybird acts as a bodyguard for the Textbook cases of bodyguard manipulation pupating wasp against predators (Maure et al., 2011). Moreover, it In contrast to most true parasites, insect parasitoids are of relatively is likely that the aposematic coloration of the ladybirds (Marples et large size and possess a free-living adult stage, and their al., 1994) operates as a complementary protection for the parasitoid, development almost universally kills the host (but see English-Loeb depending on the nature of the predators. Thus, D. coccinellae et al., 1990; Maure et al., 2011). Because of these characteristics, could also potentially usurp the natural defences of its host. behavioural modifications induced by parasitoids have evolved in a way that increases their survival during pupation (i.e. when the Indirect protection parasitoid is at its most vulnerable), through an efficient protection In contrast to the previous examples where manipulated hosts against natural enemies or abiotic factors (Poulin et al., 1994; played an active and direct role against natural enemies of the Brodeur and Boivin, 2004). The induced protection conferred by parasitoid, the following studies describe cases where the host is the host can be either direct or indirect, depending on whether the manipulated prior to parasitoid pupation in order to provide shelter onset of manipulation coincides with the period of high against potential biotic and abiotic threats. Although these vulnerability (direct protection) or occurs just before this period bodyguards do not directly face the threats, the benefits for (indirect protection). In the first case, the host is maintained alive, parasitoid survival are equally important. at least until the beginning of parasitoid pupal development, in With their studies on the aphid parasitoid nigripes, order to be used as a direct defender of the developing pupae Brodeur and McNeil tested the hypothesis that parasitic wasps against predators or hyperparasitoids (e.g. Lepidoptera hosts could avoid natural enemies in time or space through the selection attacked by a braconid wasp display aggressive responses when of suitable pupation sites by modifying the behaviour of their host disturbed; see below). In the second case, the host is manipulated (Brodeur and McNeil, 1989; Brodeur and McNeil, 1992) (Table1). just before parasitoid pupation, in such a way as to either build a Aphidius nigripes, an endoparasitoid of the potato aphid shelter or move to concealed refugia, and then is killed by the , completes its pupal development within developing parasitoid (e.g. moribund spiders parasitized by an its eviscerated host (termed ‘mummy’). Inside the mummy, the ichneumonid wasp spin a ‘cocoon web’ to favour parasitoid parasitic wasp spins a cocoon and pupates (Fig.1D). In this state, survival; see below). it remains completely defenceless as the mummy is easily torn apart by the mandibles of invertebrate predators or pierced by the Direct protection ovipositor of hyperparasitoid females. It has been shown that in The first example of this form of protection has been observed in order to enhance their survival, parasitoids have the ability to three different Lepidoptera–Braconid wasp models: Pieris modify the behaviour of M. euphorbiae, and that the induced brassicae–Cotesia glomerata (Brodeur and Vet, 1994; Harvey et behaviour differs according to the physiological state of the al., 2011), Manduca spp.–Cotesia congregata (Kester et al., 1996) parasitoid (Brodeur and McNeil, 1989; Brodeur and McNeil, 1990). and leucocerae–Glyptapanteles sp. (Grosman et al., Just prior to death, aphids containing a non-diapausing parasitoid 2008) (Table1). Female parasitic wasps deposit several eggs into leave the aphid colony and mummify on the upper surface of the the host’s haemocoel and the parasitoid larvae feed on leaves (i.e. reducing the impact of predation and hyperparasitism), host tissues throughout their development. Following egression of whereas those containing a diapausing parasitoid leave the host the parasitoid larvae from the host, the moribund caterpillar remains plant and move to more concealed sites (i.e. reducing the negative alive on the pupating parasitoids. Coiled on the cocoon masses, it effects of adverse climatic conditions and the incidence of exhibits violent head-thrashing movements, fending off predators hyperparasitism). Therefore, it seems that the pressures exerted by (Kester and Jackson, 1996; Grosman et al., 2008) or natural enemies have influenced the evolution of behavioural hyperparasitoids (Harvey et al., 2011) (Fig.1A), essentially acting modification as a means of defence. as a true bodyguard as this behaviour results in a reduction in The second example is that of ichneumonid wasps inducing their mortality of the parasitic wasp pupae. In addition to displaying this spider hosts to weave a special web for their own benefit, and is aggressive defence behaviour, it has been shown that P. brassicae documented in several associations (Nielsen, 1923; Eberhard, also spin a silk web over the parasitoid cocoons 2000; Eberhard, 2001; Matsumoto and Konishi, 2007; Matsumoto, (Fig.1B), reinforcing the physical barrier covering the parasitoid 2009; Eberhard, 2010a; Eberhard, 2010b; Gonzaga et al., 2010) pupae (Brodeur and Vet, 1994). Interestingly, these two parasite- (Table1). Female parasitoids attack a spider at the hub of its orb, induced behaviours are normal components of the host’s sting it into temporary paralysis and lay an egg on the spider’s behavioural repertoire but are usurped by the parasitoid to fulfil abdomen. Subsequently, the spider resumes normal activity while another purpose. Although the mechanisms responsible for this the wasp’s egg hatches and the larva grows by sucking the spider’s usurpation of host behaviour were not identified, they are probably haemolymph. On the night that it will kill its host, the larva induces induced by the parasitoid larvae, prior to or during egression. the spider to build a unique ‘cocoon web’ and once completed the The second example comes from our previous study (Maure et parasitoid larva moults, then kills and consumes the spider. al., 2011), describing an original model associating the parasitic Alterations of the web-spinning spider behaviour are diverse wasp Dinocampus coccinellae and one of its hosts, the spotted lady among the different ichneumonid wasps (Fig.1E–G), but they are

THE JOURNAL OF EXPERIMENTAL BIOLOGY 38 The Journal of Experimental Biology 216 (1) consistently adjusted to details of the host’s natural history (e.g. deaths, the behavioural modification observed in parasitized durable versus fragile webs, presence or absence of protected individuals is unambiguously beneficial to the parasitoid only. retreats) in ways that seem to promote the survival of the wasp’s Analogous to the strategy of aphid parasitoids (Brodeur and cocoon (Matsumoto, 2009; Gonzaga et al., 2010). Here, the McNeil, 1989; Brodeur and McNeil, 1992), by manipulating their parasitoid usurps the spider’s skill in building a sophisticated web hosts into burying themselves just prior to pupation, conopid flies but imposes new patterns, rendering it stronger and more durable. benefit from an increased protection to adverse temperature and This manipulation of the host was shown to be advantageous as it natural enemies during hibernation, resulting in higher post- confers added protection to the developing pupae from the frequent diapausing survival rates and adult size (Müller, 1994). As low heavy rains common to the areas where the species are found levels of juvenile hormone are known to induce digging behaviour (Fincke et al., 1990). in bumblebees, the authors postulated that conopid endoparasites The last example we consider here is, to our knowledge, the only are able to manipulate the production of juvenile hormone in their one involving a Diptera parasitoid. Müller investigated the digging host to induce this protective behaviour (Müller, 1994). behaviour of worker bumblebees Bombus terrestris infected with a conopid fly endoparasitoid (Müller, 1994) (Table1). Dead, Potential extensions of the bodyguard manipulation parasitized bumblebee workers were found buried in the ground Although not labelled as such, parasitic behavioural modifications significantly more often than non-parasitized ones. As the satisfying the definition of bodyguard manipulation have been bumblebees clearly gain no fitness benefits from digging to their reported in various non-parasitoid systems. An important constraint

Table 1. List of biological systems where textbook bodyguard manipulations have been reported Host–parasite systems Bodyguard behavioural alterations References Aphid–parasitic wasp Macrosiphum euphorbiae– Altered microhabitat preference in manipulated hosts results in a reduction in Brodeur and McNeil, 1989; Aphidius nigripes hyperparasitism and increased protection from adverse abiotic factors. Brodeur and McNeil, 1992 Caterpillar–parasitic wasp Pieris brassicae–Cotesia Induced web spinning and amplified aggressive/protective behaviour in manipulated Brodeur and Vet, 1994; glomerata caterpillar hosts reduce predation and hyperparasitism on parasitoid pupae. Harvey et al., 2011

Manduca spp.–Cotesia In addition to protecting parasitoid cocoons by covering them, infected caterpillars jerk Kester and Jackson, 1996 glomerata their heads backwards and spit at tachinids attempting to larviposit. Therefore, host-attached parasitoids suffer significantly less predation than parasitoids alone. Thyrinteina leucocerae– Manipulated hosts cease walking and feeding, and remain near parasitoid pupae and Grosman et al., 2008 Glyptapanteles sp. knock off predators with violent head thrashing. This modified behaviour was shown to significantly reduce the mortality from natural enemies during parasitoid pupation. Spider–parasitic wasp Plesiometa argyt– Spider hosts are induced to build an otherwise unique cocoon web to serve as a Eberhard et al., 2000; Hymenoepimecis sp. durable support for the wasp larvas cocoon in order to confer protection from the Eberhard et al., 2001 common heavy precipitation. Nephila clavipes– Parasitoid-induced alterations of the web-spinning behaviour of spiders make the Gonzaga et al., 2010 Hymenoepimecis sp. webs more resistant to destruction. The cocoon webs include a hub-like platform from which the cocoon is suspended, and are usually protected by a nearby tangle of barrier lines of variable density. Theridion evexum–Zatypota Manipulated host adds more threads on different sections of the retreat (apex, inside Weng and Barrantes, 2007 petronae and across the retreat opening), making the structure stronger and more durable. The reinforcement of the retreat with additional silk threads possibly increases protection of the cocoon against heavy rain, which is likely to be important for the wasp's survival. Cyclosa octotuberculata– The modified web is more robust and better designed to sustain the wasp's cocoon Matsumoto and Konihi, 2007 Reclinervellus sp. than the normal web. Agelena limbata– Manipulated spider hosts produce veils of very fine and dense threads covering the Matsumoto et al., 2009 Brachyzapus nikkoensis spider, and parasitoid larva were observed in the tunnel of the funnel web. The modified web seems resistant against predators and scavengers such as ants. Allocyclosa bifurca– Under the control of the parasitoid, the orb-weaving spider builds a highly modified, Eberhard, 2010b Polysphincta gutfreundi physically stable orb web, to which the larva then attaches its pupal cocoon, and adds an otherwise unsual linear silk stabilimentum to this web that may camouflage the cocoon. Anelosimus spp.–Zatypota nr. Spider hosts are induced to modify their web in such a way as to provide apparent Eberhard, 2010a solanoi protection and support for the wasp's cocoon by covering the entire web with a protective sheet and adding a central platform, and opening a space below in the enclosed tangle, where the larva suspends its cocoon. Ladybird–parasitic wasp Coleomegilla maculata– Partially paralysed on top of the parasitoid cocoon, displaying twitches when Maure et al., 2011 Dinocampus coccinellae disturbed, parasitized ladybirds act as true bodyguards. This manipulated behaviour was shown to provide an efficient protection against predators. Bumble bee–endoparasitic fly Bumbus terrestris–conopid fly Induced digging behaviour occurs in infected bumble bees. This manipulated Müller, 1994 behaviour results in the selection of a hibernation site for the parasitoid and leads to larger and heavier adult flies, showing fewer malformations in their wings than flies hibernating on the ground.

THE JOURNAL OF EXPERIMENTAL BIOLOGY Bodyguard manipulation 39

Fig.1. Illustration of bodyguard manipulation in different host species. (A)Thyrinteina leucocerae caterpillar protecting a Glyptapanteles sp. parasitic wasp cocoon (photo: J. Lino-Neto). (B)Pieris brassicae caterpillar spinning a silk web over the parasitic wasp cocoons of Cotesia glomerata (photo: Tibor B C Bukovinszky). (C)Ladybird Coleomegilla maculata attending a cocoon of the parasitic wasp Dinocampus coccinellae (photo: F.M.). (D)Mummified aphid remains, hidden under a leaf, after the emergence of the parasitic wasp Aphidius nigripes (photo: J.B.). A (E)Modified web of Nephila clavipes and a larva of the parasitic wasp F Hymenoepimecis bicolor (photo: M. Gonzaga). (F)A cocoon of the parasitic wasp Brachyzapus nikkoensis in the tunnel of the funnel web of Agelena limbata (photo: R. Matsumoto). (G)A cocoon of the parasitic wasp Hymenoepimecis sp. hanging from a modified orb web of the spider D E G Plesiometa argyta (photo: W. Eberhard). for developing parasites is that their survival in their intermediate fecundity as a consequence of the low blood intake (Rossignol et hosts is contingent on the survival of the hosts themselves. al., 1986; Koella et al., 2002). The mechanisms that control blood- Decreasing the predation risks of the intermediate hosts could be feeding behaviour in Anopheles are not completely understood, an adaptation for immature, non-infective parasites to increase their although both endocrinological and neuro-physiological fitness. For instance, within the context of multidimensional components have been detected in other mosquitoes (Lehane, 1991; manipulations (Thomas et al., 2010a) (see Appendix), there exists Clements, 1992). in certain host–parasite models a ‘bodyguard dimension’ to the Acanthocephalans have a long and well-documented history of parasite manipulation, currently termed ‘predation suppression’ by host manipulation (reviewed in Moore, 2002; Kennedy, 2006). Parker and colleagues (Parker et al., 2009). In a recent theoretical They have been shown to modify several host phenotypes model, they demonstrated that it is an evolutionary stable strategy (reviewed in Thomas et al., 2010a), serving as a prime example of for parasites to switch from predation suppression, during the non- the multidimensionality of parasitic manipulation (Thomas et al., infective phase, to predation enhancement, when the infective stage 2010b). To date, the majority of the identified phenotypic is reached and the parasite can be transmitted. Interestingly, manipulations have been linked to increased trophic transmission according to Parker and colleagues (Parker et al., 2009), this to the final host. However, alterations of the intermediate host’s parasite-induced predation suppression should evolve more easily phenotype can also potentially lead to increased predation by a than enhancement, as the former does not need to be host specific, large range of non-host predators. In a series of first-rate studies, unlike the latter. To date, there are several well-documented Médoc and colleagues (Médoc and Beisel, 2008; Médoc and Beisel, examples of such a behaviour that could be comparable to 2009; Médoc et al., 2009) identified new dimensions of bodyguard dimensions of the manipulation (Table2); we will acanthocephalan manipulation in their amphipod host. They overview two of the most compelling cases. demonstrated that the amphipod Gammarus roeseli infected with It is well established that Anopheles mosquitoes infected with the acanthocephalan Polymorphus minutus (1) had superior average the transmissible stage of the malaria parasite Plasmodium spp. and maximum swimming speeds in the presence of non-host have more frequent and longer feeding bouts than non-infected predators, (2) spent significantly more time at the air–water mosquitoes, thereby increasing parasite transmission (Koella and interface (negative geotaxis) and (3) remained significantly longer Packer, 1996; Koella et al., 1998). However, further investigation in refugia when exposed to non-host predator chemical cues, of the behaviour of parasitized mosquitoes during the non-infective compared with non-infected G. roeseli. These multiple manipulated developmental stage of the parasite’s life cycle revealed that the traits act synergistically, significantly reducing predation of parasites, in order to increase the mosquito’s survival during this infected hosts by non-host predators in both the laboratory and the non-infective period, have the capacity to manipulate their host in field. As with most host–parasite associations, the benefits a way that reduces the host’s mortality associated with blood conferred to the amphipod host in this context are outweighed by feeding (Anderson and Brust, 1996; Anderson et al., 1999). Indeed, the costs of such behaviours as parasitic manipulation invariably it has been reported that the duration and number of feeding bouts leads to complete and partial castration in the female and male are significantly lower when Plasmodium is non-infective amphipod, respectively (Ward, 1986; Bollache et al., 2001). (Anderson et al., 1999; Koella et al., 2002), suggesting that the Having overviewed some of the ‘bodyguard dimensions’, the parasite protects its host at least until its maturity. Although the host question that we now ask is, can these behavioural modifications mosquitoes benefit from an increased survivorship, their ultimate be considered as bodyguard manipulations? According to the fitness is greatly reduced, as they have significantly reduced definition proposed by Poulin, ‘a bodyguard manipulation is a

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Table 2. List of biological systems where bodyguard dimensions have been reported Host–parasite systems Bodyguard behavioural alterations References Fish–microsporidia Gasterosteus aculeatus–Glugea Increased anti-predator behaviours were observed in infected Milinski, 1985 anomala sticklebacks. Snail–trematode Potamopyrgus antipodarum– Manipulation by Microphallus sp. results in altered foraging behaviour in Levri, 1998; Levri et al., 2007 Microphallus sp. infected snail hosts. The movement of infected snails from the top to the bottom of rocks corresponds to the peak in activity of the non-host fish predator. The behavioural change was shown to reduce the probability of encounter between infected snails and fish. Mosquito–plasmodium Anopheles stephensi–Plasmodium yoelii Here, predation suppression consists of decreased feeding persistence Anderson et al., 1999 nigeriensis of female Anopheles towards a human host and was induced only by Plasmodium at oocyst stage (which cannot be transmitted). Anopheles gambiae–Plasmodium Mosquitoes infected with oocysts (which cannot be transmitted) had a Koella et al., 2002 gallinaceum smaller threshold volume and were less likely to return for further probing. Amphipod–acanthocephalan Gammarus roseli–Polymorphus minutus Despite the encystment of P. minutus in the abdomen of its intermediate Médoc and Beisel, 2008; host, infected amphipods had significantly higher swimming speeds Médoc and Beisel, 2009; than non-infected ones. Furthermore, when interacting with the non- Médoc et al., 2009 host predator, the highest escape speeds and greatest distances covered by invertebrates were observed for parasitized . Gammarus pulex–Polymorphus laevis Increased anti-predator behaviour in gammarids parasitized by the non- Dianne et al., 2011 infective stage of P. laevis (acanthella) results in a decrease in mortality by predation. Copepod–cestode Cyclops srenuus–Triaenophorus crassus Increased antipredator behaviour in infected copepod (reduced activity Hammerschmidt et al., 2009 and increased time to recover) reduces its likelihood of being eaten by the stickleback. manipulation that alters the behaviour of the host in ways that will life cycle or trophically versus not trophically transmitted) provide protection to the parasitoid pupae from predators or other constitute important selective pressures and could give rise to novel dangers’ (Poulin, 2010). But why should we limit this manipulation types of manipulation. For instance, the amphipod Gammarus to insect parasitoids? All examples described in the previous insensibilis, can be simultaneously infected by a manipulative section (including those listed in Table2) were shown to reduce trematode, Microphallus papillorobustus, that induces strong predation on the host organism or protect it from adverse behavioural alterations making them more vulnerable to predation, environmental conditions. Furthermore, the modified hosts all and by a non-manipulative nematode, Gammarinema gammari, forfeited at least one fitness-related trait as a consequence of that benefits maximally when the host behaves normally (Thomas accomplishing these behaviours. Therefore, this leads us to suggest et al., 2002a). Thomas and colleagues reported that the nematode that bodyguard manipulations have evolved across different is able to manipulate the host’s behaviour by negating the effects parasite taxa; in certain cases the induced protection conferred by of the manipulator that would lead it to an early death (Thomas et the host represents a single dimension of a more complex al., 2002a). Furthermore, in the case of parasites with simple life manipulation, and in other cases the induced protection constitutes cycles, which complete their development in one host, selection the complete manipulation. Bodyguard manipulations should be should favour any manipulative trait that would reduce host defined more generally and concern all manipulations – or mortality associated with predation. We therefore postulate that dimensions of manipulations – that alter the behaviour of the host bodyguard dimension/manipulation could have been selected for in ways that will provide protection to the parasite. within these contexts and evolved as local adaptations depending on parasitic and predator communities, even in parasites with a Evolution of bodyguard manipulations simple life cycle. In nature, all organisms cope with environmental pressures acting An important constraint for the success of this manipulation is on their survival (e.g. predation, parasitism and adverse abiotic the match between the appropriate parasite developmental stage conditions) and therefore they have evolved numerous defence and the onset of the manipulated behaviours. Within the parasitic mechanisms to reduce mortality. Parasites (developing within their wasp models that benefitted from an induced direct protection from intermediate host) and parasitoids (pupating either within or outside their host, manipulation is especially necessary at the pupal stage, their host) do not possess the ability to directly defend themselves. when parasitic wasps are particularly vulnerable to danger (Brodeur Natural selection should therefore favour manipulative parasites and Vet, 1994). For instance, in the biological model described that usurp the behaviour of their host as means of defence (Brodeur previously (Maure et al., 2011), if the paralysis of the ladybird, and McNeil, 1989; Brodeur and Vet, 1994). which inhibits ladybird foraging, is initiated prior to wasp Another possibility lies in the fact that hosts in nature are often egression, the resulting costs to the developing wasp would be parasitized by a community of phylogenetically distinct parasites, significant: (1) the already limited energetic resources within the which may have a conflict of interests (Brown, 1999; Lafferty et host would become even more limited because of the inability of al., 2000). Under such conditions, interactions between parasite the insect to feed, which would negatively affect wasp fitness; and species having different life cycles (e.g. a simple versus a complex (2) the unprotected parasitoid pupae would be completely exposed

THE JOURNAL OF EXPERIMENTAL BIOLOGY Bodyguard manipulation 41

Biological model Behavioural modifications through time Fig.A1. Schematic diagram of the two categories of multidimensional manipulations: simultaneous and sequential.

Gammarus • Positive phototactism (Helluy, 1984) insensibilis • Negative geotactism (Helluy, 1984) + • Aberrant evasive behaviour (Helluy, 1984) • Higher glycogen content (Ponton et al., 2005) Microphallus • Longer intermoult duration (Thomas et al., 1996) papillorobustus • Reduced fecundity and pairing success (Thomas et al., 1995) Simultaneous

Time

Aedes

aegypti + • Reduced appetite • Increased appetite (Koella et al., 2002) Plasmodium

Sequential gallinaceum to predation. Similarly, in parasites with complex life cycles, the Appendix induction of a bodyguard dimension is only advantageous at a The multidimensionality of parasitic manipulation precise developmental stage, prior to the parasites becoming It is increasingly recognised that parasitically modified hosts are transmissible to the next host. If predation suppression was induced not merely normal hosts with one or a few altered traits, but instead when the parasite was infective, transmission would therefore be are greatly modified organisms. Indeed, many parasites alter not greatly reduced; such behaviour should be selected against. The one but several phenotypic traits in their hosts, significantly success of this manipulation is dependent on a fixed timing of the increasing the transmission or survival of the parasite (as distinct onset of the host bodyguard behaviour. from the ‘infection syndrome’) (see Cézilly and Perrot-Minnot, 2010; Thomas et al., 2010b). Conclusions and perspectives In its most general sense, the bodyguard manipulation consists of Defining multidimensional manipulation modified host behaviours that provide protection to the developing A manipulation may be considered as multidimensional when at parasite/parasitoid against biotic or abiotic factors. Although few least two changes in different or in the same phenotypic traits are induced protective behaviours are explicitly labelled as such, this observed in manipulated hosts. These changes can occur within or original survival strategy seems to have evolved in many parasite between trait categories (behaviour, morphology and/or taxa, sometimes as a sole dimension of more complex physiology), and must not correspond to different ways of manipulations. To enhance our comprehension of the inherent measuring the same alteration. Traits that are merely host responses mechanisms governing behavioural manipulations, further should not be considered as part of multidimensional manipulation experimental evidence of efficient host protection of unless one can demonstrate that they are adaptively maintained by parasites/parasitoids is necessary. Another avenue of research that parasites because of transmission benefits. For instance, Lefèvre has already proven fruitful in a parasitoid model (Maure et al., and colleagues (Lefèvre et al., 2008) proposed that manipulative 2011) but that remains poorly understood in the context of parasites could affect fitness-related traits in their hosts (e.g. manipulative parasites in general, is the exploration of trade-offs fecundity, survival, growth) in order to stimulate host between the benefits conferred by the bodyguard manipulations and compensatory responses, when these responses match with the the direct costs to fitness-related traits (e.g. longevity, size, parasite’s transmission route. fecundity). Indeed, Parker and colleagues postulated that one of the Two categories of multidimensional manipulations have been reasons why ‘predation suppression’ is so seldom observed as observed: those where the manipulated behaviours occur compared with ‘predation enhancement’ is that suppression may be simultaneously and those where they occur sequentially. For more costly to the parasite (Parker et al., 2009). Furthermore, this example, all the behavioural changes in the amphipod host type of behaviour may also be rarely described as a consequence Gammarus insensibilis infected with the trematode Microphallus of research bias; research investigating parasitic manipulations has papillorobustus occur simultaneously, whereas the behavioural either only focused on predation enhancement rather than including changes in the mosquito vector Aedes aegypti infected with the all the dimensions of the manipulation or focused on parasites with malaria parasite Plasmodium gallinaceum appear sequentially complex life cycles as opposed to those with simple life cycles. (Fig.A1). In addition, the full understanding of these fascinating biological systems necessitates studying the mechanisms underlying host Funding manipulation. Until now, these approaches were regarded as F.M. and S.P.D. are supported by the Agence Nationale de la Recherche [Blanc unfeasible in most of the biological models that are described in SVSE7, project ʻBodyguardʼ to F.T.] and a Fondation Fyssen Postdoctoral Fellowship, respectively. the present manuscript because of the lack of molecular data in the corresponding species. But recent progress in omics approaches and the emergence of next-generation sequencing offer the References opportunity to study in detail the effect of these different parasites Anderson, R. A. and Brust, R. A. (1996). Blood feeding success of Aedes aegypti and Culex nigripalpus (Diptera: Cullicidae) in relation to defensive behavior of on their host physiology. The proliferation of these approaches in Japanese quail (Coturnix japonica) in the laboratory. J. Vector Ecol. 21, 94-104. these different models could help us to better understand the Anderson, R. A., Koella, J. C. and Hurd, H. (1999). The effect of Plasmodium yoelii nigeriensis infection on the feeding persistence of Anopheles stephensi Liston evolution of this kind of manipulation. throughout the sporogonic cycle. Proc. Biol. Sci. 266, 1729-1733.

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